Wisconsin Wildlife Project: Transmission and evolution of a persistent pathogen: anthrax infection dynamics comparing two natural systems

Wisconsin Wildlife Project

Transmission and evolution of a persistent pathogen: anthrax infection dynamics comparing two natural systems

August 2018 - September 2024

Personnel

Wendy Turner, Principal Investigator
Pauline Kamath, Co-Principal Investigator
Henriette van Heerden, Co-Principal Investigator
Yen-Hua Huang, Student / Post Doc
Zoe Barandongo, Student / Post Doc
Kimberlie Vera, Student / Post Doc
Amelie Dolfi, Student / Post Doc

Participating Agencies

University of Wisconsin - Madison

Anthrax is a globally distributed disease of wildlife, livestock, and humans. Successful prediction of and response to outbreaks of anthrax is limited by a lack of understanding of the geographic differences in the ecology of the pathogen as well as the pattern of disease outbreaks. This project will investigate the roles of host, pathogen, and environment to understand how the pathogen - host interaction evolves and contributes to the differences in anthrax occurrence between two study areas. The two areas, both in southern Africa, have very different anthrax outbreak dynamics, which are representative of variation in anthrax systems world-wide. In Etosha National Park, Namibia, there are smaller outbreaks, affecting grazing zebra, annually in wet seasons. In contrast, in Kruger National Park, South Africa, larger outbreaks affecting browsing kudu occur in dry seasons on roughly a decadal scale. The project builds on detailed records of population dynamics in each park as well as archived pathogen samples and will involve new data collection and analyses and mathematical modeling to understand these different dynamics. Education, training, and scientific and public outreach are essential components of this research. Postdoctoral researchers and undergraduate and graduate students from diverse backgrounds will be trained in field, laboratory, and quantitative techniques emphasizing cutting-edge genomics, and statistical and dynamic modeling approaches.

Research Publications

Research Publications	Publication Date
Turner, W.C., P.L. Kamath, H. van Heerden, Z. Barandongo, Y.-H. Huang, S.A. Bruce and K. Kausrud. 2021. The roles of environmental variation and parasite survival in virulence-transmission relationships. Royal Society Open Science, 8: 210088. https://doi.org/10.1098/rsos.210088 \| Abstract \| Publisher Website	June 2021	Disease outbreaks are a consequence of interactions among the three components of a host-parasite system: the infectious agent, the host, and the environment. While virulence and transmission are widely investigated, most studies of parasite life history trade-offs are conducted with theoretical models or tractable experimental systems where transmission is standardized and the environment controlled. Yet, biotic and abiotic environmental factors can strongly affect disease dynamics, and ultimately, host-parasite coevolution. Here we review research on how environmental context alters virulence-transmission relationships, focusing on the off-host portion of the parasite life cycle, and how variation in parasite survival affects the evolution of virulence and transmission. We review three inter-related “approaches” that have dominated the study of the evolution of virulence and transmission for different host-parasite systems: i) evolutionary trade-off theory, ii) parasite local adaptation, and iii) parasite phylodynamics. These approaches consider the role of the environment in virulence and transmission evolution from different angles, which entail different advantages and potential biases. We suggest improvements to how to investigate virulence-transmission relationships, through conceptual and methodological developments and taking environmental context into consideration. By combining developments in life history evolution, phylogenetics, adaptive dynamics, and comparative genomics, we can improve our understanding of virulence-transmission relationships across a diversity of host-parasite systems that have eluded experimental study of parasite life history.
Huang, Y.-H., H. Joel, M. Küsters, Z. Barandongo, C.C. Cloete, W.M. Getz, A. Hartmann, P.L. Kamath, J.W. Kilian, J.K.E. Mfune, G. Shatumbu, R. Zidon, and W.C. Turner. 2021. Disease or drought: environmental fluctuations release zebra from a potential pathogen-triggered ecological trap. Proceedings of the Royal Society of London, B. Biological Sciences, 288: 20210582. https://doi.org/10.1098/rspb.2021.0582 \| Abstract \| Publisher Website	June 2021	Habitat selection that exposes hosts to areas of high disease risk can have an adverse effect on host populations. When a transmission hotspot for an environmentally persistent pathogen establishes in otherwise high-quality habitat, the disease may exert stronger impact on the host population, and potentially forms an ecological trap. However, fluctuating environmental conditions lead to heterogeneity in habitat quality and animal habitat preference, which may interrupt the overlap between selected and risky habitats. We evaluated spatiotemporal patterns in anthrax mortalities in a plains zebra (<i>Equus quagga</i>) population in Etosha National Park, Namibia, incorporating remote-sensing and host telemetry data. A higher proportion of anthrax mortalities was detected in open habitats than in other habitat types. Resource selection functions showed that the zebra population shifted habitat selection in response to changes in vegetation productivity and rainfall. Average to high rainfall years supported larger anthrax outbreaks, with animals congregating in preferred open habitats, while a severe drought forced animals into otherwise less preferred habitats, leading to few anthrax mortalities. Thus, the timing of anthrax outbreaks was congruent with preference for open plains habitats and a corresponding increase in pathogen exposure. Given shifts in habitat preference, the overlap in high-quality habitat and high-risk habitat is intermittent, reducing the adverse consequences for the population.
Bruce, S.A., Y-H. Huang, P.L. Kamath, H. van Heerden and W.C. Turner. 2021. The roles of antimicrobial resistance, phage diversity, isolation source and selection in shaping the genomic architecture of Bacillus anthracis, Microbial Genomics, 7:000616. DOI: 10.1099/mgen.0.000616 \| Abstract \| Publisher Website	August 2021	<i>Bacillus anthracis</i>, the causative agent of anthrax disease, is a worldwide threat to livestock, wildlife and public health. While analyses of genetic data from across the globe have increased our understanding of this bacterium’s population genomic structure, the influence of selective pressures on this successful pathogen is not well understood. In this study, we investigate the effects of antimicrobial resistance, phage diversity, geography and isolation source in shaping population genomic structure. We also identify a suite of candidate genes potentially under selection, driving patterns of diversity across 356 globally extant <i>B. anthracis </i>genomes. We report ten antimicrobial resistance genes and eleven different prophage sequences, resulting in the first large-scale documentation of these genetic anomalies for this pathogen. Results of random forest classification suggest genomic structure may be driven by a combination of antimicrobial resistance, geography and isolation source, specific to the population cluster examined. We found strong evidence that a recombination event linked to a gene involved in protein synthesis may be responsible for phenotypic differences between comparatively disparate populations. We also offer a list of genes for further examination of <i>B. anthracis </i>evolution, based on high-impact single nucleotide polymorphisms and clustered mutations. The information presented here sheds new light on the factors driving genomic structure in this bacterium and may act as a road map for future studies aimed at understanding functional differences in terms of <i>B. anthracis</i> biogeography, virulence, and evolution.

Presentations

Presentations	Presentation Date
Turner, W.C. 2024. Highly persistent environmentally-mediated pathogens reveal key drivers of transmission heterogeneity. Ecology and Evolution of Infectious Diseases Annual Conference, Palo Alto, CA, 24-27 June 2024. Invited keynote talk.	June 2024

Theses and Dissertations

Theses and Dissertations	Publication Date
Zoe Barandongo. 2023. Anthrax in African wildlife: Bacillus anthracis spore survival, bacteriophages and genetic diversity in southern Africa, PhD Dissertation, University of Wisconsin - Madison	December 2023
Yen-Hua Huang. 2022. Effects of Environmental Fluctuations and Herbivore Ecology on Anthrax Dynamics in Southern Africa. Ph.D. Dissertation, University of Wisconsin-Madison.	May 2022
Sunday Ochai. 2022. Exposure to anthrax in Kruger and Etosha National Parks and the effect of haemoparasite coinfections, MS Thesis, University of Pretoria.	April 2022
Prudent Mokgokong, 2023. Comparative genomics of Bacillus anthracis strains from anthrax outbreaks in Kruger National Park, South Africa. MS Thesis, University of Pretoria	April 2023
Kamini Govender. 2023. Investigation of Bacillus anthracis spore survival in soils from Kruger National Park in South Africa and Etosha National Park in Namibia. MS Thesis, University of Pretoria	April 2023
Hendrina Joel. 2022. Effects of elephant carcasses on vegetation cover, herbivore behavior, and potential anthrax transmission in central Etosha National Park. MS Thesis, University of Namibia.	April 2022
Dolfi, A. 2024. Using simulation models to determine mechanisms driving outbreak dynamics and spatial distribution of environmentally transmitted pathogens. Ph.D. in Wildlife Ecology, University of Wisconsin - Madison.	August 2024

Data or Software Releases

Type	Citation	Publication Date
Data Release	Turner, W. C. and Barandongo, Z. R., 2023. Zebra anthrax carcass site pathogen and soil data from Namibia, 2010-2021: U.S. Geological Survey data release, https://doi.org/10.5066/P9TDAY91.	January 2023

Cooperative Fish and Wildlife Research Units Program: Wisconsin Wildlife Education, Research and Technical Assistance for Managing Our Natural Resources